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. 1983 Jan;153(1):357–363. doi: 10.1128/jb.153.1.357-363.1983

Effects of the hisT mutation of Salmonella typhimurium on translation elongation rate.

D T Palmer, P H Blum, S W Artz
PMCID: PMC217379  PMID: 6401282

Abstract

The hisT mutation in Salmonella typhimurium which results in loss of pseudouridine base modifications in the anticodon regions of many tRNAs was shown to reduce the rate of protein synthesis in vivo by about 20 to 25% as compared with that measured in hisT strains. Reduced protein synthesis rate occurred predominantly at the level of translation rather than transcription. Increased sensitivity of hisT mutants to growth inhibition by antibiotics that inhibit translation elongation, but not by those that inhibit translation initiation, transcription initiation, or transcription elongation, indicates that the hisT mutation leads to a defect in one or more of the steps in the polypeptide chain elongation mechanism. These results can account for effects of the hisT mutation on regulation of certain amino acid biosynthetic operons, including the his, leu, and ilv operons.

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Selected References

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  1. Alper M. D., Ames B. N. Transport of antibiotics and metabolite analogs by systems under cyclic AMP control: positive selection of Salmonella typhimurium cya and crp mutants. J Bacteriol. 1978 Jan;133(1):149–157. doi: 10.1128/jb.133.1.149-157.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Artz S. W., Broach J. R. Histidine regulation in Salmonella typhimurium: an activator attenuator model of gene regulation. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3453–3457. doi: 10.1073/pnas.72.9.3453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnes W. M. DNA sequence from the histidine operon control region: seven histidine codons in a row. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4281–4285. doi: 10.1073/pnas.75.9.4281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brenner M., Ames B. N. Histidine regulation in Salmonella typhimurium. IX. Histidine transfer ribonucleic acid of the regulatory mutants. J Biol Chem. 1972 Feb 25;247(4):1080–1088. [PubMed] [Google Scholar]
  5. Brenner M., Lewis J. A., Straus D. S., De Lorenzo F., Ames B. N. Histidine regulation in salmonella typhimurium. XIV. Interaction of the histidyl transfer ribonucleic acid synthetase with histidine transfer ribonucleic acid. J Biol Chem. 1972 Jul 10;247(13):4333–4339. [PubMed] [Google Scholar]
  6. Cassani G., Burgess R. R., Goodman H. M., Gold L. Inhibition of RNA polymerase by streptolydigin. Nat New Biol. 1971 Apr 14;230(15):197–200. doi: 10.1038/newbio230197a0. [DOI] [PubMed] [Google Scholar]
  7. Chang G. W., Roth J. R., Ames B. N. Histidine regulation in Salmonella typhimurium. 8. Mutations of the hisT gene. J Bacteriol. 1971 Oct;108(1):410–414. doi: 10.1128/jb.108.1.410-414.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cortese R., Landsberg R., Haar R. A., Umbarger H. E., Ames B. N. Pleiotropy of hisT mutants blocked in pseudouridine synthesis in tRNA: leucine and isoleucine-valine operons. Proc Natl Acad Sci U S A. 1974 May;71(5):1857–1861. doi: 10.1073/pnas.71.5.1857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dalbow D. G., Young R. Synthesis time of beta-galactosidase in Escherichia coli B/r as a function of growth rate. Biochem J. 1975 Jul;150(1):13–20. doi: 10.1042/bj1500013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Di Nocera P. P., Blasi F., Di Lauro R., Frunzio R., Bruni C. B. Nucleotide sequence of the attenuator region of the histidine operon of Escherichia coli K-12. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4276–4280. doi: 10.1073/pnas.75.9.4276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dube S. K., Marcker K. A., Clark B. F., Cory S. Nucleotide sequence of N-formyl-methionyl-transfer RNA. Nature. 1968 Apr 20;218(5138):232–233. doi: 10.1038/218232a0. [DOI] [PubMed] [Google Scholar]
  12. Fowler A. V., Zabin I. The amino acid sequence of beta-galactosidase of Escherichia coli. Proc Natl Acad Sci U S A. 1977 Apr;74(4):1507–1510. doi: 10.1073/pnas.74.4.1507. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Galas D. J., Branscomb E. W. Ribosome slowed by mutation to streptomycin resistance. Nature. 1976 Aug 12;262(5569):617–619. doi: 10.1038/262617b0. [DOI] [PubMed] [Google Scholar]
  14. Gorini L. Ribosomal discrimination of tRNAs. Nat New Biol. 1971 Dec 29;234(52):261–264. doi: 10.1038/newbio234261a0. [DOI] [PubMed] [Google Scholar]
  15. Gupta R. S., Schlessinger D. Coupling of rates of transcription, translation, and messenger ribonucleic acid degradation in streptomycin-dependent mutants of Escherichia coli. J Bacteriol. 1976 Jan;125(1):84–93. doi: 10.1128/jb.125.1.84-93.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hopfield J. J. Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc Natl Acad Sci U S A. 1974 Oct;71(10):4135–4139. doi: 10.1073/pnas.71.10.4135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Itikawa H., Demerec M. Salmonella typhimurium proline mutants. J Bacteriol. 1968 Mar;95(3):1189–1190. doi: 10.1128/jb.95.3.1189-1190.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Janner F., Vögeli G., Fluri R. The antisuppressor strain sin1 of Schizosaccharomyces pombe lacks the modification isopentenyladenosine in transfer RNA. J Mol Biol. 1980 May 15;139(2):207–219. doi: 10.1016/0022-2836(80)90305-8. [DOI] [PubMed] [Google Scholar]
  19. Kasai T. Regulation of the expression of the histidine operon in Salmonella typhimurium. Nature. 1974 Jun 7;249(457):523–527. doi: 10.1038/249523a0. [DOI] [PubMed] [Google Scholar]
  20. Keller E. B., Calvo J. M. Alternative secondary structures of leader RNAs and the regulation of the trp, phe, his, thr, and leu operons. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6186–6190. doi: 10.1073/pnas.76.12.6186. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kurland C. G. Structure and function of the bacterial ribosome. Annu Rev Biochem. 1977;46:173–200. doi: 10.1146/annurev.bi.46.070177.001133. [DOI] [PubMed] [Google Scholar]
  22. Lawther R. P., Hatfield G. W. Multivalent translational control of transcription termination at attenuator of ilvGEDA operon of Escherichia coli K-12. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1862–1866. doi: 10.1073/pnas.77.4.1862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Leive L. Studies on the permeability change produced in coliform bacteria by ethylenediaminetetraacetate. J Biol Chem. 1968 May 10;243(9):2373–2380. [PubMed] [Google Scholar]
  24. Lewis J. A., Ames B. N. Histidine regulation in Salmonella typhimurium. XI. The percentage of transfer RNA His charged in vivo and its relation to the repression of the histidine operon. J Mol Biol. 1972 Apr 28;66(1):131–142. doi: 10.1016/s0022-2836(72)80011-1. [DOI] [PubMed] [Google Scholar]
  25. Murray M. L., Hartman P. E. Overproduction of hisH and hisF gene products leads to inhibition of cell cell division in Salmonella. Can J Microbiol. 1972 May;18(5):671–681. doi: 10.1139/m72-105. [DOI] [PubMed] [Google Scholar]
  26. Nargang F. E., Subrahmanyam C. S., Umbarger H. E. Nucleotide sequence of ilvGEDA operon attenuator region of Escherichia coli. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1823–1827. doi: 10.1073/pnas.77.4.1823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ninio J. A semi-quantitative treatment of missense and nonsense suppression in the strA and ram ribosomal mutants of Escherichia coli. Evaluation of some molecular parameters of translation in vivo. J Mol Biol. 1974 Apr 5;84(2):297–313. doi: 10.1016/0022-2836(74)90586-5. [DOI] [PubMed] [Google Scholar]
  28. Piepersberg W., Noseda V., Böck A. Bacterial ribosomes with two ambiguity mutations: effects of translational fidelity, on the response to aminoglycosides and on the rate of protein synthesis. Mol Gen Genet. 1979 Mar 9;171(1):23–34. doi: 10.1007/BF00274011. [DOI] [PubMed] [Google Scholar]
  29. Putnam S. L., Koch A. L. Complications in the simplest cellular enzyme assay: lysis of Escherichia coli for the assay of beta-galactosidase. Anal Biochem. 1975 Feb;63(2):350–360. doi: 10.1016/0003-2697(75)90357-7. [DOI] [PubMed] [Google Scholar]
  30. Rosenfeld S. A., Brenchley J. E. Regulation of nitrogen utilization of hisT mutants of Salmonella typhimurium. J Bacteriol. 1980 Aug;143(2):801–808. doi: 10.1128/jb.143.2.801-808.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schleif R., Hess W., Finkelstein S., Ellis D. Induction kinetics of the L-arabinose operon of Escherichia coli. J Bacteriol. 1973 Jul;115(1):9–14. doi: 10.1128/jb.115.1.9-14.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Scott J. F., Roth J. R., Artz S. W. Regulation of histidine operon does not require hisG enzyme. Proc Natl Acad Sci U S A. 1975 Dec;72(12):5021–5025. doi: 10.1073/pnas.72.12.5021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sippel A., Hartmann G. Mode of action of rafamycin on the RNA polymerase reaction. Biochim Biophys Acta. 1968 Mar 18;157(1):218–219. doi: 10.1016/0005-2787(68)90286-4. [DOI] [PubMed] [Google Scholar]
  34. Smith H. O., Levine M. A phage P22 gene controlling integration of prophage. Virology. 1967 Feb;31(2):207–216. doi: 10.1016/0042-6822(67)90164-x. [DOI] [PubMed] [Google Scholar]
  35. Turnbough C. L., Jr, Neill R. J., Landsberg R., Ames B. N. Pseudouridylation of tRNAs and its role in regulation in Salmonella typhimurium. J Biol Chem. 1979 Jun 25;254(12):5111–5119. [PubMed] [Google Scholar]
  36. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  37. Zengel J. M., Young R., Dennis P. P., Nomura M. Role of ribosomal protein S12 in peptide chain elongation: analysis of pleiotropic, streptomycin-resistant mutants of Escherichia coli. J Bacteriol. 1977 Mar;129(3):1320–1329. doi: 10.1128/jb.129.3.1320-1329.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]

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